JOURNAL OF PLANT PROTECTION RESEARCH
Vol. 55, No. 3 (2015)
DOI: 10.1515/jppr-2015-0038
Fusarium head blight (FHB) and Fusarium spp. on
grain of spring wheat cultivars grown in Poland
Leszek Lenc1*, Grzegorz Czecholiński2, Dariusz Wyczling3,Tomasz Turów3,
Arkadiusz Kaźmierczak1
1 Department
of Molecular Phytopathology, University of Technology and Life Sciences in Bydgoszcz,
Kordeckiego 20, 85-225 Bydgoszcz, Poland
2 Experimental Station for Variety Testing in Lisewo Malborskie, Kolejowa 43, 82-224 Lichnowy, Poland
3 ProCam Polska Sp. z o.o., Nowy Świat 42/44, 80-299 Gdańsk, Poland
Received: April 9, 2015
Accepted: June 17, 2015
Abstract: Eighteen spring wheat cultivars, recommended for commercial production in northern Poland, were assessed for Fusarium
head blight (FHB) in natural non-epidemic conditions, from 2011 to 2013. Assessment was based on FHB incidence (proportion of
heads with symptoms), disease severity (DS; proportion of bleached spikelets per head), proportion of Fusarium damaged kernels
(FDK), and spectrum of Fusarium spp. colonising the kernels. Fusarium head blight incidence and DS often differed significantly
among cultivars and years. There was a strong positive correlation between FHB incidence and DS. Fusarium head blight incidence
and DS were not correlated with the June–July temperatures, and were only occasionally correlated with the total June–July rainfall.
There was a weak positive correlation between FHB incidence and proportion of FDK. There was a strong positive correlation between DS and proportion of FDK. The cultivar affected colonisation of kernels by Fusarium spp. Fusarium poae was the FHB pathogen
isolated most often. Fusarium poae colonised 6.0% of the kernels, on average, but up to 12.0% on individual cultivars. Other Fusarium
species were less frequent: F. avenaceum in 5.6% of kernels, F. culmorum in 5.3%, F. tricinctum in 2.8%, F. graminearum in 1.5%, and F. sporotrichioides in 1.2%. Fusarium equiseti occurred sporadically. The importance of F. poae in the FHB complex is emphasised. All cultivars
expressed ‘moderate FHB resistance’ if evaluated according to FHB incidence. Cultivars Arabella, Izera, Kandela, Monsun, Ostka
Smolicka, and Struna expressed ‘moderate susceptibility’, and Bombona, Hewilla, Katoda, KWS Torridon, Łagwa, Nawra, Parabola,
Radocha, SMH 87, Trappe, Tybalt, and Waluta expressed ‘susceptibility’ if evaluated by the proportion of FDK. Cultivars differed
within the ‘moderately resistant’, ‘moderately susceptible’, and ‘susceptible’ categories. Cultivars Arabella, Izera, Kandela, Monsun,
Ostka Smolicka, and Struna were the most promising and their resistance traits may be useful in FHB management.
Key words: cultivar, Fusarium, Fusarium head blight (FHB), spring wheat, susceptibility
Introduction
Spring wheat is the second most valuable cereal after
winter wheat. It is grown in Poland on 380 000 ha, particularly in the north and in Lower Silesia (southern Poland). The area has increased recently because of losses
occurring in winter crops. Spring wheat’s advantages
make it popular in large-scale and commercial production, and locally on ecological farms.
Spring wheat cultivars bred in Europe are characterised by short, lodging-resistant stalks (usually decreasing FHB, which can be more severe in crops that lodge),
higher yields, and high efficiency in mineral nutrition.
The quality of the grain depends on the genetic features
of the cultivar, weather conditions, and agricultural management. Spring wheat may have less yield than its winter equivalent. Instead, the popularity of spring wheat
results from its agricultural value. Spring wheat has
a shorter period of growth and of exposure to pathogens,
*Corresponding address:
[email protected]
pests, and weeds. All of these features decrease cultivation costs.
Fusarium head blight (FHB) is one of the most important cereal diseases. It has emerged as a major threat to
wheat and barley crops around the world. Fusarium head
blight contributes to loss of grain yield and quality due to
colonisation by Fusarium fungi and contamination with
mycotoxins (Siuda et al. 2010; Grabowski et al. 2012a, b;
Gromadzka et al. 2012).
The prevalence of disease depends on agronomic
practices, effectiveness of fungicides used, and host resistance. In Poland, FHB has been observed every year with
differences in incidence. In some years, incidence was
low (< 1% of heads colonized). Recently, FHB severity has
increased, and has been seen each year on approximately
70% of wheat fields (Wakuliński et al. 1991; Lenc et al.
2011; Sadowski et al. 2011; Lenc 2015).
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Fusarium head blight (FHB) and Fusarium spp. on grain of spring wheat cultivars grown in Poland
Seventeen species of Fusarium, with different climatic
requirements and genetic and environmental adaptations, contribute to disease (Parry et al. 1995; Stępień and
Chełkowski 2010; Wiśniewska et al. 2014). Fusarium graminearum Schwabe [Gibberella zeae (Schwein.) Petch] is
the predominant causal agent of FHB in most areas. This
fungus is the most virulent worldwide. In Poland, FHB is
caused mostly by F. culmorum (Wm. G. Sm.) Sacc., F. avenaceum (Fr.) Sacc. (Gibberella avenacea R.J. Cook) and F. poae
(Peck) Wollenw. (Wakuliński and Chełkowski 1993; Lenc
2015). The contribution of particular species to FHB incidence depends on habitat and weather conditions.
Deoxynivalenol (DON) and zearalenone are the most
common mycotoxins associated with FHB They pose a serious threat to human and domestic animal health. Crop
sequence and tillage (which incorporates crop residues
into the soil) have been shown to affect the incidence of
FHB. In recent years, decreased tillage is thought to have
contributed to regional epidemics by increasing the levels
of inoculum available for infection. Additionally, disease is
favored by extended periods of moderately high temperature (15–30°C), high moisture (relative humidity > 90%),
and frequent rainfall (De Wolf et al. 2003; Lemmens et al.
2004; Xu et al. 2008; Sadowski et al. 2011; Lenc 2015).
Extensive research aimed at controlling FHB has focused on the development of wheat cultivars resistant
to Fusarium spp. and the use of such resistant cultivars
in integrated management systems. The development
of resistant cultivars is the most effective, economic,
and environmentally safe way to control FHB in wheat.
Thousands of plant lines are subjected to artificial inoculation with Fusarium spp. (mostly with F. graminearum).
Those lines having reduced fungal growth and low levels
of seed contamination with DON, are selected and advanced in further breeding trials. Quantitative Trait Loci
(QTL) composed of one or more genes, such as Fhb1 derived from the Chinese wheat cultivar Sumai 3, have been
identified and widely used in wheat breeding (Steiner et
al. 2004; Góral 2005; Zhang et al. 2008; Kubo et al. 2013).
Two main types of resistance to FHB are widely accepted: Type I, resistance to initial infection; and Type II,
resistance to fungal spread within the spike (Schroeder
and Christensen 1963). Three other types of resistance
were reported by Mesterhazy et al. (1999): Type III, resistance to DON accumulation; Type IV, resistance to
kernel infection; Type V, tolerance. Infection and disease
development can be affected by both active (i.e. physiological processes) and passive (i.e. plant height, spike
architecture, flowering date) resistance factors that are
difficult to separate (Crute et al. 1985; Mesterhazy 1995;
Buerstmayr et al. 2009). Integrated management of FHB
in wheat depends on disease forecasting models which
help to determine the risk of FHB infection and optimise
the agronomic and chemical control of disease. The risk
of FHB infection depends partly on cultivar resistance to
Fusarium spp., which must be considered in commercial
production. Genetic variability is essential for the development of FHB resistant cultivars. Sources of FHB resistance/tolerance in spring wheat have so far been introduced from China, Brazil, Europe, and Japan (Fedak et al.
267
2001). There is always a chance of finding further sources
of resistance in local cultivars and lines.
The objective of this study was to assess: (i) FHB incidence and disease severity in 18 cultivars of spring wheat
grown in a conventional system in northern Poland in the
2011–2013 time period; (ii) effects of weather conditions
on FHB incidence and severity; (iii) populations of Fusarium fungi involved in FHB, and hence, implications for
human and domestic animal mycotoxicoses; (iv) suitability of particular spring wheat cultivars for FHB resistance
breeding, commercial production, and requirements of
integrated management. The objectives are of particular
significance in terms of the European Commission Regulation No. 856/2005 of 6 June 2005 regarding food safety
and Fusarium toxin concentrations in food and feed.
Materials and Methods
Site description
Seventeen common spring wheat (Triticum aestivum L.)
cultivars (Arabella, Bombona, Hewilla, Izera, Kandela,
Katoda, KWS Torridon, Łagwa, Monsun, Nawra, Ostka
Smolicka, Parabola, Radocha, Struna, Trappe, Tybalt, and
Waluta) from elite groups (A–E), and one durum spring
wheat (T. turgidum ssp. durum) cultivar (SMH 87) were
grown in a conventional system in experimental fields
at the Experimental Station for Variety Testing in Lisewo
Malborskie, northern Poland (54° 6’ N, 18° 43’ E) from
2011 to 2013. Not all cultivars were grown in each of the
study years. The experiment was established with four
replicates in a randomised block design in brown soil of
class I quality. The chemical characteristics of the soil at
Lisewo (2011–2013) are presented in table 1. The previous crop in each year was the sugar beet (Beta vulgaris L.).
Sowing was done on 8–10 April at 450–500 grains ∙ m–2.
Fertiliser application each year was: 140 kg NH4+ ∙ ha–1,
70 kg P2O5 ∙ ha–1 and 100 kg K2O ∙ ha–1. Fungicidal seed
treatments, and herbicide and insecticide sprays were applied each year (Table 2). Grain was harvested each year
on 27–30 August.
The average 2011–2013 temperatures in June were
15.5–17.8°C, and in July 18.3–18.6°C, with the highest
temperatures in July 2012 (Table 3). Total rainfall in June
was from 36.2 to 125.1 mm, and in July from 102.3 to
170.3 mm, with the most rain in July 2013. The number of
days with rain was in the range of 8–18 in June, and 12–20
in July. Although temperatures were moderate in June–
July 2011–2013, the high rainfall in June 2012 and July
2011–2013, and the high number of days with rainfall,
particularly in July 2011–2013, meant that weather conditions were generally favorable for FHB development.
Collection of samples and disease assessment
Each year (2011–2013), 50 heads of wheat from each cultivar were collected at late milk to early dough development stages (GS 77-83; Zadoks et al. 1974). These wheat
heads were collected from randomly chosen plants along
a diagonal transect across each of the four replicate plots.
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268
Journal of Plant Protection Research 55 (3), 2015
Table 1. Chemical characteristics of soil at Lisewo, in 2011–2013
Soil characteristics
2011
2012
2013
pH in KCl
5.9
5.8
6.2
Extractable soil phosphorus [mg ∙ kg–1]a
9.9
24.4
18.2
Extractable soil potassium [mg ∙ kg–1]b
17.8
20.0
25.1
Extractable soil magnesium [mg ∙ kg–1]b
12.6
12.4
13.5
aanalysed
banalysed
with the Egner-Riehm method
with the Schachtschabel method
Table 2. Pesticides used in spring wheat production at Lisewo, in 2011–2013
Seed treatment
2011
2012
2013
Fungicide
Sarfun T 65 DS1
(200 g ∙ 100 kg–1)
Sarfun T 65 DS
(200 g ∙ 100 kg–1)
Zaprawa T 75DS/WS2
(200 g ∙ 100 kg–1)
Herbicide
Gold 450 EC3 + Gallaper 200 EC4
(1.0 l + 0.8 l ha–1)
Granstar Ultra5 + Tomigan 250 EC6
(40 g + 0.5 l ha-1)
Granstar Ultra + Hurler 200 EC7
(40 g + 0.4 l ha–1)
Insecticide
Karate Zeon 050CS8
(0.12 l ∙ ha–1)
Karate Zeon 050CS
(0.1 l ∙ ha–1)
Wojownik 050SC9
(0.1 l ∙ ha–1)
1Carbendazim
20% + thiuram 45%; 2Thiuram 75%; 3Terbuthrine + metolachlor; 4Fluoroxypyr; 5Tribenuron methyl 50% + trisodium
phosphate dodecahydrate 20%; 6Fluroxypyr 25%; 7Fluroxypyr meptyl 20%; 8Lambda-cyhalothrin + 1,2-benzisothiazolin-3-one;
9Lambda cyhalothrin 5%
Table 3. Temperature and rainfall during the flowering and ripening stages of spring wheat growth at Lisewo, in 2011–2013
(according to Experimental Station for Variety Testing in Lisewo Malborskie)
Month
June
July
10-day period
Total rainfall
[mm]
Average temperature [°C]
Number of days with rainfall
2011
2012
2013
2011
2012
2013
I
19.1
13.0
15.8
9.1
16.7
5.6
3
6
2
II
16.5
16.9
18.7
18.1
24.9
0.5
4
6
2
III
17.7
16.8
17.8
11.7
83.5
30.1
2
6
4
average
17.8
15.5
17.4
38.9
125.1
36.2
9
18
8
I
17.6
20.0
18.2
47.0
60.6
88.8
6
8
4
II
19.4
16.2
17.4
45.9
23.8
38.2
6
8
4
III
18.2
19.6
19.4
15.2
17.9
43.3
6
4
4
average
18.4
18.6
18.3
108.1
102.3
170.3
18
20
12
verity, were evaluated visually on 200 heads from each
cultivar. Fusarium head blight incidence was determined
as the proportion (%) of heads with symptoms. Disease
severity (DS), i.e. the extent of head damage (%), was
determined as the proportion of bleached spikelets per
head, based on a 1–9 scale: 1 – no symptoms; 2 – < 5% of
bleached spikelets; 3 – 5–15%; 4 – 16–25%; 5 – 26–45%; 6 –
46–65%; 7 – 66–85%; 8 – 86–95%; 9 – 96–100% (Miedaner
and Perkowski 1996).
Colonisation of wheat kernels by fungi
Mycological analysis of 400 (4 × 100) wheat kernels collected randomly during harvest from the four plots of
each cultivar was performed each of the study years. In
the laboratory, the kernels were rinsed for 45 min in run-
2011
2012
2013
ning water, disinfected in 1% NaOCl solution for 2.5 min,
rinsed three times for 10 min in sterile distilled water, and
placed on Potato Dextrose Agar (PDA; boiled and sieved
white potatoes 400 g ∙ l–1, agar 20 g ∙ l–1, streptomycin
50 mg ∙ l–1, pH = 7) in Petri dishes. Fungi were incubated
for 7–10 days at 20°C in a day-night cycle. All colonies on
each plate were then examined macro- and microscopically and distinguished on the basis of colour, growth
rate, hyphal characteristics, and sporulation. Colonies of
each species were counted and representative fungi were
identified by morphotyping on PDA and Synthetic Nutrient Agar (SNA; KH2PO4 1 g ∙ l–1, KNO3 1 g ∙ l–1, MgSO4 ∙
∙ 7H2O 0.5 g ∙ l–1, KCl 0.5 g ∙ l–1, glucose 0.2 g ∙ l–1, sucrose
0.2 g ∙ l–1) using Booth (1971), Kwaśna et al. (1991). Proportions (%) of Fusarium-colonised kernels (FDK) were
calculated.
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Fusarium head blight (FHB) and Fusarium spp. on grain of spring wheat cultivars grown in Poland
269
Evaluation of cultivar response to Fusarium infection
Colonisation of kernels by Fusarium spp.
The response of each cultivar was determined from
FHB incidence and the proportion of FDK. For response
based on the FHB incidences (proportion of heads with
symptoms), the following scale was used: 0 – immune;
1–5% – resistant; 5–25% – moderately resistant; 25–50%
– moderately susceptible; 50–75% – susceptible; > 75% –
very susceptible. For response based on the proportion
of FDK, the scale was as follows: 0 – immune; 1–8% –
resistant; 9–11% – moderately resistant; 12–20% – moderately susceptible; 21–50% – susceptible; > 50% – very
susceptible.
Cultivar affected the colonisation of kernels by Fusarium
spp. There were significant differences in proportions
of FDK in cultivars in each of the years of the study
(Table 5). Averaged over three years, FDK ranged from
13.0% (cv. Izera) to 35.3% (cv. Tybalt). In cvs Katoda, KWS
Torridon, Monsun, Parabola, Radocha, SMH 87, Struna,
Trappe, and Tybalt, the high average (2011–2013) FDK
(20.0–35.3%) was associated with a high average FHB incidence (10.0–16.3%). In cvs Arabella, Izera, and Kandela,
the lower average (2011–2013) FDK (13.0–16.8%) was associated with a lower average FHB incidence (6.7–9.5%).
The average FDK of all cultivars was similar in all the
years of the study. There was a weak, but significant,
positive correlation between proportion of FDK and FHB
incidence (r = 0.594, p ≤ 0.001) and a stronger positive correlation between proportion of FDK and DS (r = 0.733,
p ≤ 0.001). There was a weak, but significant, negative correlation between total rainfall in July and the proportion
of FDK (r = – 0.636, p ≤ 0.001).
Statistical analysis
The statistical significance of differences in FHB incidence and in DS on different cultivars was tested using
one-way analysis of variance (ANOVA, p ≤ 0.05) and
Tukey’s post hoc test, (FR-ANALWAR software). Percentage values were transformed into Bliss degrees before
statistical analysis. The statistical significance of differences in the number of FDK and the statistical significance of differences in the number of kernels colonised
by individual Fusarium species were determined using
χ2 tests. The null hypothesis assumed that wheat from
different systems had the same number of kernels colonised by Fusarium spp. Pearson’s correlation coefficient
was applied to analyse the relationships between FHB
incidence, DS, proportion of FDK, yield, temperature,
and rainfall.
Results
Effects of cultivar on disease
Fusarium head blight (FHB) incidence and DS differed
among cultivars and years, often significantly (Table 4).
Differences were not usually consistent. In 2011, there
was no FHB on cvs Kandela, Łagwa or Ostka Smolicka,
and the most FHB was on cvs Parabola (11.5%) and Tybalt (9.5%). There was more FHB in 2012 and 2013. In
2012, the least FHB incidence occurred on cv. Trappe
(7%) and the most on cvs Bombona, Izera, Kandela,
Katoda, KWS Torridon, Tybalt, and Waluta (10.5–14%).
In 2013, a low FHB incidence (6.5–10%) was observed
on a few cultivars including Arabella (6.5%) and most
occurred again on cv. Tybal (25.5%). There was strong
positive correlation between FHB incidence and DS
(r = –0.925, p ≤ 0.001).
Effects of weather on disease
In 2011, 2012, and 2013, FHB incidence and DS were not
correlated with the June–July temperatures. Fusarium
head blight incidence was not correlated with total rainfall. Only DS was correlated, at a low level, with July
rainfall (r = 0.516–0.657, p ≤ 0.001). June rainfall was least
in 2011 and 2013 but was associated with lower average
FHB and DS values only in 2011.
Fungal species in kernels
Cultivar significantly affected colonisation of kernels
by individual Fusarium species (χ2 test, p ≤ 0.05). Fusarium poae was the Fusarium species isolated most often
(Table 6). It was frequent each year, on each cultivar. It
colonised 6.0% of the kernels, on average, but up to 12.0%
on cv. Tybalt. Other Fusarium species occurred less frequently: F. avenaceum (G. avenacea) in 5.6% of kernels, on
average, F. culmorum in 5.3%, F. tricinctum (G. tricincta) in
2.8%, F. graminearum (G. zeae) in 1.5%, and F. sporotrichioides in 1.2% of kernels. Fusarium equiseti (G. intricans) was
the rarest. Wheat kernels were also colonised by other
fungi; the most common were Alternaria alternata, Arthrinium phaeospermum, and Epicoccum nigrum.
Yield
The total grain yield or thousand-kernel weight (TKW)
was not affected by FHB incidence. There was no correlation between average yield of individual cultivars or average TKW in 2011–2013, and average FHB incidence, DS
or proportion of FDK. Average grain yield of individual
cultivars in 2011–2013 ranged from 6.09 t ∙ ha–1 (cv. SMH
87) to 9.41 t ∙ ha–1 (cv. Trappe) (Table 7). The range of the
average TKW was from 44.8 g (cv. Trappe) to 56.0 g (cv.
Parabola). There was a weak, but significant, negative
correlation between average yield of individual cultivars
in 2011–2013 and TKW (r = –0.639, p ≤ 0.001). The highest yields, in cvs Trappe (9.41 t ∙ ha–1) and KWS Torridon
(9.32 t ∙ ha–1), were associated with the lowest TKW (44.8 g
and 45.9 g, respectively) (Table 8). The lowest yield, in cv.
SMH 87 (6.09 t ∙ ha–1), was associated with high TKW
(53.2 g), and high FHB incidence (13.5%) and DS (5.2%).
Cultivar response to Fusarium infection
All cultivars expressed ‘moderate resistance’ when assessed according to the FHB incidence (Table 8). Cultivars
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270
Journal of Plant Protection Research 55 (3), 2015
Table 4. Fusarium head blight (FHB) incidence and disease severity (DS) on different cultivars of spring wheat at Lisewo, in 2011–2013
Cultivar
FHB [%]
DS [%]
2011
2012
Arabella
–
10.0a,b,c,d
Bombona
5.0b,c
12.5a,b
10.0c,d,e,f
Hewilla
4.0c
8.0c,d
10.0c,d,e,f
7.5e,f
Izera
2013
6.5f
2011–2013
2011
2012
18.3b,c,d,e
–
4.1b,c,d
2.3i
9.2b,c,d
2.3a,b,c
5.5a,b
4.1e,f,g,h
7.3c,d,e,f
2.2b,c
3.4c,d
3.7f,g,h,i
4.6a,b,c,d
2.6h,i
–
11.5a,b,c
Kandela
0.0d
11.0a,b,c
9.0d,e,f
Katoda
7.5a,b,c
11.0a,b,c
13.0b,c,d
10.5a,b,c
–
10.5a,b,c,d
13.0b,c,d
111.8a,b,c
0.0d
7.5c,d
8.5d,e,f
5.3f
KWS Torridon
Łagwa
Monsun
–
–
Nawra
9.0a,b
–
Ostka Smolicka
0.0d
Parabola
11.5a
8.0c,d
11.0b,c,d,e,f
2013
2011–2013
13.2c,d,e,f,g
19.5a,b,c
–
6.7d,e,f
0.0c
4.7a,b,c
3.4g,h,i
4.2a,b
4.6a,b,c,d
4.7d,e,f,g
–
4.4a,b,c,d
5.3c,d,e
5.5a,b
3.0h,i
211.0a,b,c
0.0c
–
–
0.0c
6.4a
15.5b,c
113.5a,b
14.0b,c,d
111.5a,b,c
2.8e,f,g
–
5.7e,f
3.2c,d
4.5b,c,d,e,f
14.9a,b,c,d
–
9.0d,e,f
–
2.7f,g
5.0a,b
29.0b,c,d
3.1d,e,f,g
13.6c,d,e,f,g
3.6f,g,h,i
–
4.0c,d,e,f,g
23.6c,d,e,f,g
25.0a,b,c,d
3.4g,h,i
2.2g
–
6.2b,c
16.3a,b
–
3.8b,c,d
5.8b,c,d
14.8b,c,d,e
–
–
5.2c,d,e
25.2a,b,c
4.0e,f,g,h
24.0c,d,e,f,g
15.0a,b,c,d
Radocha
–
9.0b,c,d
SMH 87
–
–
13.5b,c,d
213.5a,b
10.0c,d,e,f
210.0a,b,c
–
–
111.8a,b,c
–
2.9d
7.0b
5.1a,b
6.1a
9.6a
6.9a
2.1b,c
4.6a,b,c,d
5.0c,d,e,f
3.9c,d,e,f,g
Struna
–
–
Trappe
–
7.0d
16.5b
Tybalt
9.5a
14.0a
25.5a
Waluta
4.0c
11.0a,b,c
12.0b,c,d,e
Average
5.1
10.1
12.0
16.3a
9.0b,c,d
10.0
Least significant difference (LSD) at p = 0.05
2.7
4.4
4.6
4.2
4.13
1.78
1.57
2.02
1data
from two years
from one year
A different letters in a column indicates significant difference according to one-way ANOVA at p ≤ 0.05
2data
Table 5. Proportion (%) of Fusarium damaged kernels (FDK) in different cultivars of spring wheat at Lisewo, in 2011–2013
Cultivar
2011
2012
Arabella
–
17.0f
13.0g,h
Bombona
22.0c,d
22.0c,d,e,f
21.0c,d,e,f
21.7e,f,g
Hewilla
31.0a,b
20.0e,f
22.0b,c,d,e,f
24.3c,d,e
–
16.0f
10.0h
Kandela
16.5d
18.0e,f
16.0f,g
Katoda
35.0a
30.0a,b
27.0b,c
24.0b,c,d,e
22.0b.c,d,e,f
21.0d,e,f
10.0h
Izera
KWS Torridon
Łagwa
Monsun
–
36.0a
2013
2011–2013
115.0i,j
113.0j
16.8h,i
30.7b
123.0d,e,f
22.3d,e,f,g
–
–
Nawra
25.5b,c
–
Ostka Smolicka
26.0b,c
20.0e,f
12.0g,h
Parabola
29.0a,b
–
26.0b,c,d
127.5b,c
Radocha
–
25.0b,c,d,e
126.0c,d
223.0d,e,f
27.0a,b,c,d
20.0d,e,f
–
SMH 87
–
–
23.0b,c,d,e
Struna
–
–
Trappe
–
220.0f,g,h
225.5c,d,e
19.3f,g,h
19.0e,f
219.0g,h
28.0a,b,c
28.0b
128.0b,c
Tybalt
34.0a
32.0a
40.0a
35.3a
Waluta
29.5a,b
22.0c,d,e,f
22.0b,c,d,e,f
24.5c,d,e
Average
28.5
22.8
20.9
23.1
1data
from two years
from one year
A different letters in a column indicates significant difference according to χ2 test at p ≤ 0.05
2data
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0
0
0
Periconia macrospinosa Lefebvre & Aar.G. Johnson
Trichoderma viride Pers.
Sterile mycelia
0
0.3
0
1.3
1.7
6.0
0.7
1.0
1.3
0
0
0.3
3.0
0
6.7
1.0
27.3
0.7
2.0
3.0
1.0
0
9.0
65.0
1.0
1.5
5.3
0
5.7bc
0.3
5.2cd
6.3bc
Hewilla
0
1.5
1.0
0
4.5
0.5
3.0
2.5
Izera1
0.5
1.0
0
1.5
0.5
2.0
1.5
23.5
2.5
0.5
4.0
1.0
0.5
4.5
61.5
from two years ; 2data from one year
A different letters in a row indicates significant difference according to χ2 test at p ≤ 0.05
3.5
Penicillium spp..
1data
1.0
Microdochium bolleyi (R. Sprague) de Hoog & Herm.-Nijh.
1.0
1.0
3.5
Epicoccum nigrum Link
Khuskia oryzae H.J. Huds.
0.5
17.5
Cladosporium herbarum (Pers.) Link
Melanospora damnosa (Sacc.) Lindau
30.0
1.0
0
0
3.7
62.3
3.5
63.5
Alternaria alternata (Fr.) Keissl.
2.0
Botrytis cinerea Pers.
1.0
Acremoniella fusca (Kunze & J.C. Schmidt) Sacc.
1.0
Bipolaris sorokiniana (Sacc.) Shoemaker
1.5
G. zeae (Schwein.) Petch
2.0
1.0
2.0
1.0
G. tricincta El-Gholl, McRitchie, Schoult. & Ridings
1.0
0.5
G. intricans Wollenw.
3.7d
1.2
Aureobasidium pullulans (de Bary & Löwenthal) G. Arnaud
2.5
Gibberella avenacea R.J. Cook
Aspergillus niger Tiegh.
1.5
F. sporotrichioides Sherb.
7.0c
7.5
5.5
F. poae (Peck) Wollenw.
5.8c
Bombona
Arthrinium phaeospermum (Corda) M.B. Ellis
2.5
Arabella1
Fusarium culmorum (W.G. Sm.) Sacc.
Taxon
Kandela
6.3
60.0
1.0
0.7
0.3
0
2.7
1.0
4.7
1.7
29.0
0.3
2.0
2.3
0.7
0
1.7
5.0
0.7
7.0ab
2.3
5.8c
8.2ab
Katoda
1.0
0
0
1.3
1.7
4.3
1.3
30.7
0
2.3
0
1.0
0
4.7
58.7
1.0
Others fungi
1.3
2.3
0
5.8bc
0.3
4.0d
3.0d
KWS Torridon1
1.0
0
0
0.5
0
2.5
2.5
20.0
0
1.5
1.5
1.0
0
8.5
69.0
0.5
4.5
1.0
0
4.5
0.5
5.5
7.0
0
1.0
0
2.0
1.7
7.3
1.3
25.3
0.7
1.0
1.0
1.0
0.7
6.7
61.3
2.0
1.2
4.2
0
3.7d
2.0
9.3b
2.0d
Łagwa
Table 6. Average proportion (%) of kernels colonised by fungi in different cultivars of spring wheat at Lisewo, in 2011–2013
Monsun2
0
0
0
0
0
6.0
1.0
19.0
1.0
0
2.0
0
1.0
9.0
68.0
0
2.0
2.0
1.0
11.0e
2.0
1.0e
1.0
Nawra2
1.0
0
0
1.0
0
7.0
1.0
29.0
0
1.0
1.0
0
0
11.0
68.0
5.0
0
6.0
0
5.0
4.5
9.0c
1.0
Ostka Smolicka
0
0
0.3
4.3
1.3
6.7
1.0
29.3
1.7
1.0
0.7
1.3
0
7.0
60.3
3.0
0
4.7
0
5.7bc
0.8
5.7cd
2.5
Parabola1
0
0
0
2.0
0
4.0
0.5
22.0
0
1.0
1.5
0
0
11.0
61.0
1.0
1.5
4.0
0
4.3d
2.8
8.0c
7.0
Radocha1
1.0
0
0
1.5
4.0
3.5
22.0
0.5
1.0
3.5
1.5
0
5.5
60.0
2.0
2.5
2.5
0.5
4.5d
0
8.0c
8.0
SMH 872
0
0
0
0
1.0
7.0
1.0
10.0
2.0
1.0
3.0
0
1.0
9.0
66.0
0
0
2.0
1.0
8.0ab
0
2.0e
9.0
Struna2
0
2.0
0
2.0
1.0
2.0
1.0
22.0
2.0
1.0
2.0
0
1.0
8.0
60.0
1.0
1.0
1.0
1.0
6.0bc
0
5.0
5.0
Ttrappe1
0
0.5
0
1.0
0.5
0
0
0
1.0
0.3
4.0
1.7
0.5
3.5
22.0
1.0
0.7
0
0.7
0
9.0
55.3
0.3
2.0
3.8
0.7
5.0cd
1.3
12.0a
10.5a
Tybalt
22.5
0
2.5
0.5
1.0
0
8.0
62.0
3.0
1.0
0.5
0
5.0
1.0
8.5c
12.0
Waluta
0
0.3
0.3
2.0
1.0
7.3
1.0
22.7
0.3
1.7
1.3
0.7
0.3
7.0
66.0
3.0
2.3
3.2
0
8.3a
1.0
7.0c
2.7d
Fusarium head blight (FHB) and Fusarium spp. on grain of spring wheat cultivars grown in Poland
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271
272
Journal of Plant Protection Research 55 (3), 2015
Table 7. Grain yield and thousand kernel weight (TKW) in different cultivars of spring wheat at Lisewo, in 2011–2013 (according to
the Experimental Station for Variety Testing in Lisewo Malborskie)
Yield [t ∙ ha-1]
Cultivar
TKW [g]
2011
2012
2013
average
2011–2013
2011
2012
2013
average
2011–2013
Bombona
8.04
9.29
9.22
8.85
49.0
46.6
42.4
46.0
Hewilla
8.21
8.81
8.77
8.59
54.0
50.5
46.6
50.4
–
8.91
8.95
8.93
–
48.6
43.9
46.3
Kandela
8.04
9.29
9.22
8.85
52.4
51.7
47.1
50.4
Katoda
8.46
9.10
8.68
8.74
53.6
48.7
47.1
49.8
–
9.87
8.77
9.32
–
45.3
46.4
45.9
Łagwa
8.12
8.62
9.22
8.65
53.8
49.7
50.3
51.3
Ostka Smolicka
8.80
8.62
8.41
8.61
54.4
47.6
47.3
49.8
Parabola
8.12
–
–
8.12
56.0
–
–
56.0
Radocha
8.12
8.14
–
8.13
55.2
51.7
–
53.5
SMH 87
6.09
–
–
6.09
53.2
–
–
53.2
Struna
–
–
9.04
9.04
–
–
45.5
45.5
Trappe
8.97
10.15
9.13
9.41
49.6
44.5
40.3
44.8
Tybalt
8.63
9.48
9.22
9.11
54.0
50.0
47.2
50.4
Waluta
7.87
8.43
8.50
8.26
51.2
48.5
46.5
48.7
Izera
KWS Torridon
Table 8. Resistance category of spring wheat cultivars determined from assessments, in 2011–2013
Cultivar response
Cultivar
FHB [%]
FDK [%]
moderately susceptible
8.3
15.0
moderately resistant
susceptible
9.2
21.7
Hewilla
moderately resistant
susceptible
7.3
24.3
Izera
moderately resistant
moderately susceptible
9.5
13.0
Kandela
moderately resistant
moderately susceptible
6.7
16.8
Katoda
moderately resistant
susceptible
10.5
30.7
KWS Torridon
moderately resistant
susceptible
11.8
23.0
Łagwa
moderately resistant
susceptible
5.3
22.3
Monsun
moderately resistant
moderately susceptible
11.0
20.0
Nawra
moderately resistant
susceptible
9.0
25.5
Ostka Smolicka
moderately resistant
moderately susceptible
5.7
19.3
Parabola
moderately resistant
susceptible
13.5
27.5
Radocha
moderately resistant
susceptible
11.5
26.0
SMH 87
moderately resistant
susceptible
13.5
23.0
Struna
moderately resistant
moderately susceptible
10.0
19.0
Trappe
moderately resistant
susceptible
11.8
28.0
Tybalt
moderately resistant
susceptible
16.3
35.3
Waluta
moderately resistant
susceptible
9.0
24.5
based on FHB incidence
based on FDK
Arabella
moderately resistant
Bombona
FHB – Fusarium head blight; FDK – Fusarium-colonised kernels
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Fusarium head blight (FHB) and Fusarium spp. on grain of spring wheat cultivars grown in Poland
Arabella, Izera, Kandela, Monsun, Ostka Smolicka, and
Struna expressed ‘moderate susceptibility’ and cvs Bombona, Hewilla, Katoda, KWS Torridon, Łagwa, Nawra,
Parabola, Radocha, SMH 87, Trappe, Tybalt, and Waluta
expressed ‘susceptibility’ when assessed by proportion of
FDK. Cultivars differed in their levels of ‘moderate resistance’, ‘moderate susceptibility’, and ‘susceptibility’.
Discussion
Growing wheat cultivars with greater resistance to FHB
is the most promising strategy for disease control. Fusarium head blight resistance is, however, a complex trait. To
date, sources of resistance conferring complete resistance
to FHB have not been identified in wheat. Resistance to
FHB has been shown to be under the control of a few major QTLs operating together with unknown numbers of
minor genes (Buerstmayr et al. 2009; Kollers et al. 2013).
Reported sources of FHB resistance in spring wheat
include a few landraces, ‘Sumai 3’ and its derivatives
from China, ‘Nobeoka Bozu’ and ‘Sin Chunaga’ and its
relatives from Japan, and ‘Frontana’ and ‘Encruzilhada’
from Brazil (Mesterhazy 1987; Liu and Wang 1991; Ban
and Suenaga 2000; Yu et al. 2006).
Most success has been made in transferring FHB resistance from the Chinese wheat cultivar Sumai 3 (Anderson
et al. 2001, 2007; Rudd et al. 2001). Cultivar Sumai 3 has
the FHB resistance gene Fhb1, which has been extensively
used in breeding programs as a major source of partial
resistance to FHB. It showed a major effect on Type II resistance across different genetic backgrounds and environments. Other QTLs for FHB resistance have exhibited
minor effects and their expression varied significantly.
Heavy use of narrow FHB resistance sources may increase selection pressure on the pathogens to erode the
efficacy of the resistance genes involved. Thus, identification and characterisation of additional sources of resistance are important for enhancing the level of resistance
and for introducing genetic variation to the breeding materials. Evaluation of FHB resistance in local cultivars of
spring wheat may provide: (i) good lines for local breeding programmes and (ii) selected resistant cultivars for
commercial farming aimed at production of mycotoxinfree grain in integrated FHB management systems based
on forecasting models.
Spring wheat cultivars in Europe have the highest levels of resistance to FHB when compared with cultivars
from South America or Asia (Zhang et al. 2008). Polish cultivars and foreign cultivars/lines have been continuously
screened for FHB resistance (Góral 2005; Wiśniewska and
Kowalczyk 2005; Lenc and Sadowski 2011; Góral and
Walentyn-Góral 2014). Research has also concentrated on
how the previous crop and weather conditions affect infection by Fusarium, and on concentrations of mycotoxins
in grain (Sadowski et al. 2011; Góral et al. 2012). The most
resistant genotypes, with acceptable agronomic characters, are used in farming and breeding, often despite the
failure to identify their sources of resistance.
The results reported here showed significant differences in FHB incidence among spring wheat cultivars
included in the Polish National List of Agricultural Plant
273
Varieties, in natural non-epidemic conditions, in northern
Poland, from 2011 to 2013. The official catalogues of varieties describe the FHB resistance of particular cultivars
as average (cv. Łagwa), moderate (cvs Arabella, Hewilla,
Kandela, Katoda, KWS Torridon, Monsun, Nawra, Ostka
Smolicka, Parabola, Radocha, SMH 87, Trappe, Tybalt,
and Waluta) or very good (cvs Bombona, Izera, and Struna). The average FHB severity, which in Lisewo ranged
from 2.2–6.9%, is consistent with the general resistance
to Fusarium spp., which would have contributed to the
2011–2013, non-epidemic situatioIt should be noted, that
there were significant differences within this ‘general
resistance’. Only cv. Tybalt had FHB severity (DS) approaching 7%, which is the lower limit for light epidemics
(Del Ponte et al. 2005). The cultivars compared were being recommended for commercial production in northern
Poland in 2014 (Anonymous 2014). Cultivars Bombona,
Hewilla, Kandela, Katoda, Łagwa, Monsun, Nawra Ostka
Smolicka, Parabola, Trappe, and Waluta were also being
used for the production of seeds. Each cultivar was on
an area of 51–445 ha (Góral and Walentyn-Góral 2014).
Choosing more susceptible cultivars would be associated
with a greater risk of Fusarium mycotoxin contamination,
a decreased germination rate, and poor seedling growth
(Gilbert and Tekauz 1995). The use of infected grain can,
by addition of virulent toxigenic biotypes of fungi, additionally enrich the complex of soil phytopathogens associated with seedling blight.
Fusarium head blight (FHB) is a major fungal disease
in durum wheat. Fewer sources of resistance have been
found in tetraploid durum wheat than in hexaploid wheat
(Rudd et al. 2001; Oliver et al. 2008). There was high FHB
incidence (13.5%) and disease severity (5.2%) in the single
durum wheat cultivar (SMH 87) that we tested. The high
FHB incidence was associated with the smallest grain
yield (6.09 t ∙ ha–1). Durum wheat is said to be susceptible
mostly to F. graminearum (G. zeae). It was suggested by
Lionetti et al. (2015) that content and composition of cell
wall polymers affect susceptibility to the wall-degrading
enzymes produced by F. graminearum during infection,
which affects the outcome of host-pathogen interactions.
This fungus was not found in cv. SMH 87. Infected kernels were colonised mostly by G. avenacea.
Resistance of Type I (to initial infection), Type II (to
spread within the head) and Type IV (to kernel infection) to FHB, were assessed in this study. Types I and II
were assessed from FHB incidence and DS on developing heads, and Type IV from the proportion of FDK as
suggested by Mesterhazy et al. (1999). Type III resistance
(resistance to DON accumulation) is also said to be an important component of FHB resistance (Miller et al. 1985;
Snijders and Perkowski 1990) but was not included in our
study. Fusarium head blight incidence is not always correlated with DON concentration (Mesterházy et al. 1999;
Bai et al. 2001; Koch et al. 2006; Brennan et al. 2007; Lehoczki-Krsjak et al. 2010; Wegulo et al. 2011; Gromadzka
et al. 2012). It was assumed here, that cultivars with low
kernel colonisation by Fusarium spp. had low concentrations of mycotoxins and stable FHB resistance (Snijders
and Krechting 1992; Bai et al. 2001).
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274
Journal of Plant Protection Research 55 (3), 2015
The assessments based on FHB incidence and DS confirmed general ‘moderate FHB resistance’ of the cultivars
included in the study. The category ‘moderately resistant’
is based, however, on a wide range (5–25%) of FHB incidence values. On this basis, expression of resistance
within the ‘moderate resistance’ category, was greatest in
cvs Arabella, Bombona, Hewilla, Izera, Kandela, Łagwa,
Nawra, Ostka Smolicka, Struna, and Waluta (FHB = 5.3–
10.0%, DS = 2.2–5.0%). Less resistance in this ‘moderate
resistance’ category was expressed by cvs Katoda, KWS
Torridon, Monsun, Parabola, Radocha, SMH 87, Trappe,
and Tybalt (FHB = 10.5–16.3%, DS = 3.6–6.9%). On the basis of the proportion of FDK, the cultivars were categorised as ‘moderately susceptible/susceptible’, i.e. with
lower levels of resistance. These assessments of cultivar
response to Fusarium infection in the field differ from the
results of Zhang et al. (2008). They found that European
cultivars of spring wheat with ‘moderate resistance’ in
the field displayed higher levels of resistance based on
the proportion of FDK.
There was a positive correlation between FHB incidence and the proportion of FDK. In more resistant cultivars, there was less kernel colonisation. An explanation
is that limited fungal colonisation of kernels in resistant
cultivars results from membrane-based tolerance of
trichothecene mycotoxins (Snijders and Krechting 1992).
However, a lack of significant correlation between FHB
incidence and the proportion of FDK has also been reported, and attributed to two different sources of resistance (Sneller et al. 2012).
None of the cultivars in the present study was highly
resistant to FHB. This is partly in agreement with Góral
and Walentyn-Góral (2014) who found statistically significant variability in FHB resistance and a wide range
of FHB incidences among 25 spring wheat cultivars
from the Polish National List and 35 cultivars/lines from
a collection of resistant forms over a three-year study
(2010–2012). They found moderate FHB resistance in cvs
Bombona, Łagwa, Monsun, Ostka Smolicka, Trappe, and
Waluta, and greater resistance in cvs Hewilla, Kandela,
Katoda, Nawra, and Parabola.
Fusarium poae, F. avenaceum, and F. culmorum were
the most frequent Fusarium spp. in spring wheat kernels.
They were also the most frequent in a study on winter
wheat in Poland (Lenc et al. 2011; Lenc 2015). These species, together with F. graminearum, F. pseudograminearum
O’Donnell & T. Aoki (teleomorph Gibberella coronicola T.
Aoki & O’Donnell), Microdochium nivale (Fr.) Samuels &
I.C. Hallett (teleomorph Monographella nivalis (Schaffnit)
E. Müll.), and M. majus (Wollenw.) Glynn & S.G. Edwards, form the dominant group in FHB populations in
Europe, USA, and Canada (Wilcoxon et al. 1988; Gale et
al. 2007; Alvarez et al. 2010). Fusarium avenaceum, F. culmorum, and F. poae are more adapted to cooler/wet/humid
regions (Doohan et al. 2003), although Xu et al. (2008) also
associated F. poae with relatively drier and warmer conditions. According to Rohácik and Hudec (2005), a high
incidence and density of F. poae in warmer places results
from its adaptability to agro-environmental conditions
during grain formation.
In general terms, F. poae and F. avenaceum are relatively weaker pathogens than F. graminearum and F. culmorum (Wong et al. 1992; Fernandez and Chen 2005; Xu et
al. 2007). Only individual isolates of F. poae are strongly
aggressive (comparable with F. culmorum and F. graminearum) (Brennan et al. 2007). It is receiving increased
interest because of its toxigenic potential (it produces
trichothecenes of types A and B, aurofusarin, beauvericin, butenolide, culmorin, cyclonerodiol, enniatins, fusarin, and moniliformin) and the human and animal mycotoxicoses it can cause (De Nijs et al. 1996a, b; Thrane et al.
2004; Chełkowski et al. 2007).
Fusarium graminearum was relatively rare in the spring
wheat cultivars although its increasing contribution to
FHB in Poland has been observed (Czaban et al. 2011;
Lenc 2015). In general, F. graminearum favors warmer
weather. The increasing significance of F. graminearum is
related to global warming (higher temperatures in spring
and summer) and increased amounts of maize residues
and fungal inoculum associated with increased production of maize for grain (Wakuliński and Chełkowski
1993). Fusarium langsethiae Torp and Nirenberg, a species
with increasing significance in Poland (Łukanowski et al.
2008; Łukanowski and Sadowski 2008), was not recorded.
The colonisation of kernels by other pathogenic or saprotrophic fungi may increase the likelihood of further
deterioration and additional chemical contamination of
the grain. The taxa recorded (Table 6) are often known to
be secondary invaders, which can cause serious storage
mold problems. Alternaria, Aspergillus, and Penicillium
spp. are known mycotoxin producers (Steyn 1995). Their
presence in grain constitutes a potential additional health
risk. Storage of cereals under warm and humid conditions may further increase mycotoxin content even when
field infections were only light to moderate. Trichoderma
viride, which is antagonistic towards Fusarium spp. with
a potential to reduce inoculum development (Inch and
Gilbert 2007), occurred sporadically.
The studies were carried out in only one location, but
the complexity of resistance mechanisms and significant
environment effects on FHB development require screening in a range of environments (Fuentes et al. 2005). The
location in northern Poland, however, is in the main target
area for spring wheat production because of the weather
conditions. In addition, the ‘moderately resistant’ categorisation of the cultivars chosen for study ensures that
they should have some stability under different epidemic
conditions. According to Mesterházy (1995), the stability of plant reaction is connected to the resistance level;
the most resistant genotypes are the most stable, and the
most susceptible ones tend to be unstable.
Weather is usually the main determinant of FHB incidence (Parry et al. 1995; De Wolf et al. 2003; Lemmens
et al. 2004; Xu et al. 2008). Epidemics of FHB are associated with multiple inoculation episodes and with coincidental wet periods. Higher humidity favors the growth
and sporulation of Fusarium fungi which are spread by
wind and rain splashes. Lower humidity helps plants to
dry and prevents infection and colonisation. In this study,
though, a decreased average proportion of FDK was observed with increased rainfall in July. There was intense
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Fusarium head blight (FHB) and Fusarium spp. on grain of spring wheat cultivars grown in Poland
and prolonged rain in July 2011–2013. Rain intensity, duration, and frequency, as well as the size and velocity of
falling drops, affect the splash dispersal of spores and
success of infection (Shin et al. 2014). Intense rain may
have a decreased effective dispersal by washing off newly-dispersed spores, which therefore, did not contribute
to increased Fusarium infection (Penet et al. 2014). Wind
will increase primary rain-dispersal distance in a downwind direction and decrease it upwind, although it is accepted that wind-dispersal distances are generally longer
than rain dispersal alone, and that pure splash dispersal
is mostly local (Yang et al. 1990; Sache 2000). The epidemiology of FHB caused by F. poae and the pathogenś infection biology are less understood then other major FHB
patogens (Stenglein 2009).
Conclusions
Eighteen spring wheat cultivars were all found to be
‘moderately resistant’ to ‘moderately susceptible’ to FHB
in non-epidemic situations in the field. There were differences within the wide range of resistance/susceptibility
categories. The cultivars showing most resistance (Arabella, Izera, Kandela, Monsun, Ostka Smolicka, and Struna) can be recommended for breeding programmes and
for commercial farming with the aim of producing mycotoxin-free grain in integrated FHB management systems.
Acknowledgements
The authors thank the Head of the Experimental Station
for Variety Testing in Karżniczka for his cooperation in
allowing this research to be carried out on the premises.
This research was supported by the University of
Technology and Life Sciences in Bydgoszcz, BS 8/2012
“Pathogenic and nonpathogenic fungi in the natural environment“.
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